1887

Abstract

The effects of octyl gallate on yeast cells were analysed in relation to its capacity to oxidize compounds (pro-oxidant actions). All phenolic compounds tested inhibited the alternative oxidase (AOX). However, only octyl gallate induced a morphological change in yeast cells and collapsed the mitochondrial membrane potential. In contrast to octyl gallate, propyl gallate and nordihydroguaiaretic acid caused only a negligible cell change and the membrane potential was not affected. Our findings show that structurally related phenolic compounds do not necessarily exert similar actions on target cells. Preincubation of cells with trolox inhibited the change to pseudohyphal growth produced by octyl gallate. These results suggest that in addition to the inhibitory action of octyl gallate on the AOX, this compound induces a switch from yeast to a mycelium, probably through the formation of lipid peroxides.

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2009-02-01
2019-12-12
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References

  1. Akerboom, T. P. & Sies, H. ( 1981; ). Assay of glutathione, glutathione disulfide and glutathione mixed disulfides in biological samples. Methods Enzymol 77, 373–382.
    [Google Scholar]
  2. Akerman, K. E. O. & Wikström, M. K. F. ( 1976; ). Safranine as a probe of the mitochondrial membrane potential. FEBS Lett 68, 191–197.[CrossRef]
    [Google Scholar]
  3. Akhter, S., McDade, H. C., Gorlach, J. M., Heinrich, G., Cox, G. M. & Perfect, J. R. ( 2003; ). Role of alternative oxidase gene in pathogenesis of Cryptococcus neoformans. Infect Immun 71, 5794–5802.[CrossRef]
    [Google Scholar]
  4. Bölker, M., Genin, S., Lehmier, C. & Kahmann, R. ( 1995; ). Genetic regulation of mating, and dimorphism in Ustilago maydis. Can J Bot 73, 320–325.[CrossRef]
    [Google Scholar]
  5. Boyd, I. & Beveridge, E. G. ( 1979; ). Relationship between the antibacterial activity towards Escherichia coli NCTC 5933 and the physico-chemical properties of some esters of 3,4,5-trihydroxybenzoic acid (gallic acid). Microbios 24, 173–184.
    [Google Scholar]
  6. Brzhevskaia, O. N., Kayushin, L. P. & Nedelina, O. S. ( 1966; ). On the existence of free radicals in the enzymatic hydrolysis of adenosine triphosphate (ATP). Biofizika 11, 213–216.
    [Google Scholar]
  7. D'Souza, C. A. & Heitman, J. ( 2001; ). Conserved cAMP signaling cascades regulate fungal development and virulence. FEMS Microbiol Rev 25, 349–364.[CrossRef]
    [Google Scholar]
  8. Fujita, K. & Kubo, I. ( 2002a; ). Plasma membrane injury induced by nonyl gallate in Saccharomyces cerevisiae. J Appl Microbiol 92, 1035–1042.[CrossRef]
    [Google Scholar]
  9. Fujita, K. & Kubo, I. ( 2002b; ). Antifungal activity of octyl gallate. Int J Food Microbiol 79, 193–201.[CrossRef]
    [Google Scholar]
  10. Hirasawa, M. & Takada, K. ( 2004; ). Multiple effects of green tea catechin on the antifungal activity of antimycotics against Candida albicans. J Antimicrob Chemother 53, 225–229.[CrossRef]
    [Google Scholar]
  11. Inoue, M., Suzuki, R., Koide, T., Sakaguchi, N., Ogihara, Y. & Yabu, Y. ( 1994; ). Antioxidant, gallic acid, induces apoptosis in HL-60RG cells. Biochem Biophys Res Commun 204, 898–904.[CrossRef]
    [Google Scholar]
  12. Jensen, E. C., Ogg, C. & Nickerson, K. W. ( 1992; ). Lipoxygenase inhibitors shift the yeast/mycelium dimorphism in Ceratocystis ulmi. Appl Environ Microbiol 58, 2505–2508.
    [Google Scholar]
  13. Juárez, O., Guerra, G., Martinez, F. & Pardo, J. P. ( 2004; ). The mitochondrial respiratory chain of Ustilago maydis. Biochim Biophys Acta 1658, 244–251.[CrossRef]
    [Google Scholar]
  14. Juárez, O., Guerra, G., Velázquez, I., Flores-Herrera, O., Rivera-Pérez, R. E. & Pardo, J. P. ( 2006; ). The physiologic role of alternative oxidase in Ustilago maydis. FEBS J 273, 4603–4615.[CrossRef]
    [Google Scholar]
  15. Jürgensen, C. W., Jacobsen, N. R., Emri, T., Eriksen, S. H. & Pocsi, I. ( 2001; ). Glutathione metabolism and dimorphism in Aureobasidium pullulans. J Basic Microbiol 41, 131–137.[CrossRef]
    [Google Scholar]
  16. Kahmann, R., Steinberg, G., Basse, C., Feldbrügge, M. & Kämper, J. ( 2000; ). Ustilago maydis, the causative agent of corn smut disease. In Fungal Pathology, pp. 347–371. Edited by J. W. Kronstad. Dordrecht: Kluwer Academic Publishers.
  17. Kim, J. H., Campbell, B. C., Mahoney, N., Chan, K. L. & May, G. S. ( 2006; ). Targeting antioxidantive signal transduction and stress response system: control of pathogenic Aspergillus with phenolic that inhibit mitochondrial function. J Appl Microbiol 101, 181–189.[CrossRef]
    [Google Scholar]
  18. Klose, J., Moniz, M. & Kronstad, J. W. ( 2004; ). Lipid-induced filamentous growth in Ustilago maydis. Mol Microbiol 52, 823–835.[CrossRef]
    [Google Scholar]
  19. Koide, T., Nose, M., Yabu, Y. & Ohta, N. ( 1998; ). Trypanocidal effects of gallic acid and related compounds. Planta Med 64, 27–30.[CrossRef]
    [Google Scholar]
  20. Kubo, I. ( 1999; ). Molecular design of antioxidant and antimicrobial agents. Chemtech 29, 37–42.
    [Google Scholar]
  21. Maeta, K., Nomura, W., Takatsume, Y., Izawa, S. & Inoue, Y. ( 2007; ). Green tea polyphenols function as prooxidants to activate oxidative stress responsive transcription factors in yeast. Appl Environ Microbiol 73, 572–580.[CrossRef]
    [Google Scholar]
  22. Martínez-Espinoza, A. D., León, C., Elizarraraz, G. & Ruiz-Herrera, J. ( 1997; ). Monomorphic nonpathogenic mutants of Ustilago maydis. Phytopathology 87, 259–265.[CrossRef]
    [Google Scholar]
  23. Martinez-Espinoza, A. D., Garcia-Pedrajas, M. & Gold, S. E. ( 2002; ). The Ustilaginales as plant pests and model systems. Fungal Genet Biol 35, 1–20.[CrossRef]
    [Google Scholar]
  24. Martínez-Espinoza, A. D., Ruiz-Herrera, J., León-Ramírez, C. G. & Gold, S. E. ( 2004; ). MAP kinase and cAMP signaling pathways modulate the pH-induced yeast-to-mycelium dimorphic transition in the corn smut fungus Ustilago maydis. Curr Microbiol 49, 274–281.[CrossRef]
    [Google Scholar]
  25. Miyoshi, H., Tsujishita, H., Tokutake, N. & Fujita, T. ( 1990; ). Quantitative analysis of uncoupling activity of substituted phenols with a physicochemical substituent and molecular parameters. Biochim Biophys Acta 1016, 99–106.[CrossRef]
    [Google Scholar]
  26. Nakagawa, Y. & Tayama, S. ( 1995; ). Cytotoxicity of propyl gallate and related compounds in rat hepatocytes. Arch Toxicol 69, 204–208.[CrossRef]
    [Google Scholar]
  27. Nakagawa, Y., Moldés, P. & Moore, G. ( 1997; ). Propyl gallate-induced DNA fragmentation in isolated rat hepatocytes. Arch Toxicol 72, 33–37.[CrossRef]
    [Google Scholar]
  28. Nakayama, T., Hiramitsu, M., Osawa, T. & Kawakishi, S. ( 1993; ). The protective role of gallic acid esters in bacterial cytotoxicity and ROS responses induced by hydrogen peroxide. Mutat Res 303, 29–34.[CrossRef]
    [Google Scholar]
  29. Penninckx, M. J. & Elskens, M. T. ( 1993; ). Metabolism and functions of glutathione in microorganisms. Adv Microb Physiol 34, 239–301.
    [Google Scholar]
  30. Roy, G., Lombardia, M., Palacis, C., Serrano, A., Cespón, C., Ortega, E., Eiras, P., Luján, S., Revilla, Y. & González-Porqué, P. ( 2000; ). Mechanistic aspect of induction of apoptosis by lauryl gallate in murine B-cell lymphoma line Wehi 231. Arch Biochem Biophys 383, 206–214.[CrossRef]
    [Google Scholar]
  31. Ruiz-Herrera, J., León, C. G., Guevara-Olvera, L. & Cárabez-Trejo, A. ( 1995; ). Yeast–mycelial dimorphism of haploid and diploid strains of Ustilago maydis in liquid culture. Microbiology 141, 695–703.[CrossRef]
    [Google Scholar]
  32. Serrano, A., Palacios, C., Roy, G., Cespon, C. & González-Porqué, P. ( 1998; ). Derivatives of gallic acid induce apoptosis in tumoral cell lines and inhibit lymphocyte proliferation. Arch Biochem Biophys 350, 49–54.[CrossRef]
    [Google Scholar]
  33. Shi, L. & Pardini, R. S. ( 1995; ). Effect of NDGA on beef heart mitochondria and EMT6 mouse mammary carcinoma cells. Res Commun Mol Pathol Pharmacol 90, 235–254.
    [Google Scholar]
  34. Shimoji, H. & Yamasaki, H. ( 2005; ). Inhibitory effects of flavonoids on alternative respiration of plant mitochondria. Biol Plant 49, 117–119.[CrossRef]
    [Google Scholar]
  35. Siedow, J. N. & Grivin, M. E. ( 1980; ). Alternative respiratory pathway. Its role in seed respiration and its inhibition by propyl gallate. Plant Physiol 65, 669–674.[CrossRef]
    [Google Scholar]
  36. Tanton, L. L., Nargang, C. E., Kessler, K. E., Li, Q. & Nargang, F. E. ( 2003; ). Alternative oxidase expression in Neurospora crassa. Fungal Genet Biol 39, 176–190.[CrossRef]
    [Google Scholar]
  37. Thomas, D., Klein, K., Manavathu, E., Dimmock, J. R. & Mutus, B. ( 1991; ). Glutathione levels during thermal induction of the yeast-to-mycelial transition in Candida albicans. FEMS Microbiol Lett 61, 331–334.
    [Google Scholar]
  38. Williams, R. J., Spencer, J. P. & Rice-Evans, C. ( 2004; ). Flavonoids: antioxidants or signaling molecules? Free Radic Biol Med 36, 838–849.[CrossRef]
    [Google Scholar]
  39. Yoshino, M., Haneda, M., Naruse, M., Htay, H. H., Iwata, S., Tsubouchi, R. & Murakami, K. ( 2002; ). Prooxidant action of gallic acid compounds: copper-dependent strand breaks and the formation of 8-hydroxy-2′-deoxyguanosine in DNA. Toxicol In Vitro 16, 705–709.[CrossRef]
    [Google Scholar]
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